Analysis of the conformational change of myosin during ATP hydrolysis using fluorescence resonance energy transfer

Journal of Biochemistry

Volumn 132, Issue 3, 2002, Pages 471-482

  Mizukura, Yoshiaki ^a   Maruta, Shinsaku ^a  

^a SOKA UNIVERSITY   (Japan)

Author keywords

Energy transduction; Fluorescent ATP analog; FRET; Myosin

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; MYOSIN; FLUORESCENT DYE;

ANIMAL TISSUE; ARTICLE; CHICKEN; ENERGY TRANSFER; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; MUSCLE CONTRACTION; NONHUMAN; PROTEIN CONFORMATION; SKELETAL MUSCLE; CHEMISTRY; ION EXCHANGE CHROMATOGRAPHY; METABOLISM;

ANIMALIA; GALLUS GALLUS;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; CHROMATOGRAPHY, DEAE-CELLULOSE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ENERGY TRANSFER; FLUORESCENCE; FLUORESCENT DYES; HYDROLYSIS; MYOSINS; PROTEIN CONFORMATION;

EID: 0036739603     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.jbchem.a003245     Document Type: Article

References (79)

1. Mueller, H. and Perry, S.V. (1965) Characterization of the molecular region containing the active sites of myosin. J. Biol. Chem. 240, 3816-3828
2. Cooke, R., Crowder, M.S., Wendt, C.H., Bamett, V.A., and Thomas, D.D. (1984) Muscle cross-bridges: do they rotate? Adv. Exp. Med. Biol. 170, 413-427.
3. Vebert, P. and Cohen, C. (1988) Domains, motions and regulation in the myosin head. J. Muscle Res. Cell Motil. 9, 296-305
4. Werber, M.M., Szent-Gyorgye, A.G., and Fasman, G.D. (1972) Fluorescence studies on heavy meromyosin-substrate interaction. Biochemistry 11, 2872-2883
5. Bagshaw, C.T., Eccelston, J.F., Ekstein, F., Goody, R.S., Gutfreund, H., and Trentham, D.R. (1974) The magnesium ion-dependent adenosine triphosphatase of myosin. Two-step processes of adenosine triphosphate association and adenosine diphosphate dissociation. Biochem. J. 141, 351-364
6. Rosenfeld, S.S. and Taylor, E.W. (1984) Reactions of 1-N6-ethanoadenosine nucleotides with myosin subfragment 1 and actosubfragment 1 of skeletal and smooth muscle. J. Biol. Chem. 259, 11908-11919
7. Woodward, S.K., Geeves, M.A., and Manstein, D.J. (1995) Kinetic characterization of the catalytic domain of Dictyostelium discoideum myosin. Biochemistry 34, 16056-16064
8. Kurzawa, S.E. and Geeves, M.A. (1996) A novel stopped-flow method for measuring the affinity of actin for myosin head fragments using microgram quantities of protein. J. Muscle Res. Cell Motil. 17, 669-676
9. Kurzawa, S.E., Manstein, D.J., and Geeves, M.A. (1997) Dictyostelium discoideum myosin II: characterization of functional myosin motor fragments. Biochemistry 36, 317-323
10. Cremo, C.R. and Geeves, M.A. (1998) Interaction of actin and ADP with the head domain of smooth muscle myosin: implications for strain-dependent ADP release in smooth muscle. Biochemistry 37, 1969-1978
11. Goodno, C.C. (1979) Inhibition of myosin ATPase by vanadate ion. Proc. Natl. Acad. Sci. USA 76, 2620-2624
12. 19F NMR, J. Biol. Chem. 268, 7093-7100
13. Werber, M.M., Peyser, Y.M., and Muhlrad, A. (1992) Characterization of stable beryllium fluoride, aluminum fluoride, and vanadate containing myosin subfragment 1-nucleotide complexes. Biochemistry 31, 7190-7197
14. Phan, B. and Reisler, E. (1992) Inhibition of myosin ATPase by beryllium fluoride. Biochemistry 31, 4787-4793
15. Gopal, D. and Burke, M. (1995) Formation of stable inhibitory complexes of myosin subfragment 1 using fluorescandium anions. J. Biol. Chem. 270, 19282-19286
16. Maruta, S., Uyehara, Y., Homma, K., Sugimoto, Y., and Wakabayashi, K. (1999) Formation of the myosin-ADP-gallium fluoride complex and its solution structure by small-angle synchrotron X-ray scattering. J. Biochem. 125, 177-185
17. n ternary complex by fluorescent probes and small-angle synchrotron X-ray scattering. J. Biochem. 128, 687-94
18. Park, S., Ajtai, K., and Burghardt, T.P. (1999) Inhibition of myosin ATPase by metal fluoride complexes. Biochim. Biophys. Acta 1430, 127-140
19. -. Biochemistry 34, 8960- 8972
20. Smith, C.A. and Rayment, I. (1996) X-ray structure of the magnesium (II).ADP. vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 Å resolution. Biochemistry 35, 5404-5417
21. Rayment, I., Rypniewski, W.R., Schmidt-Base, K., Smith, R., Tomchick, D.R., Benning, M.M., Winkelmann, D.A., Wasenberg, G., and Holden, H.M. (1993) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261, 50-58
22. Katayama, E. (1989) The effects of various nucleotides on the structure of actin-attached myosin subfragment-1 studied by quick-freeze deep-etch electron microscopy. J. Biochem. 106, 751-770
23. Katayama, E. (1998) Quick-freeze deep-etch electron microscopy of the actin-heavy meromyosin complex during the in vitro motility assay. J. Mol. Biol. 278, 349-367
24. Ito. K., Liu. X., Katayama, E., and Uyeda, T.Q.P. (1999) Cooperativity between two heads of dictyostelium myosin II in in vitro motility and ATP hydrolysis. Biophys. J. 76, 985-992
25. Wakabayashi, K., Tokunaga, M., Kohno, I., Sugimoto, Y., Hamanaka, T., Takezawa, Y., Wakabayashi, T., and Amemiya, Y. (1992) Small-angle synchrotron x-ray scattering reveals distinct shape changes of the myosin head during hydrolysis of ATP. Science 258, 443-447
26. Lowey, S., Waller, G.S., and Trybus, K.M. (1993) Skeletal muscle myosin light chains are essential for physiological speeds of shortening. Nature 365, 454-456
27. Whittaker, M., Wilson-Kubalek, E.M., Smith, J.E., Faust, L., Milligan, R.A., and Sweeney, H.L. (1995) A 35-A movement of smooth muscle myosin on ADP release. Nature 378, 748-751
28. Rayment, I. (1996) The structural basis of the myosin ATPase activity. J. Biol. Chem. 271, 15850-15853
29. Uyeda, T.Q.P., Abramson, P.D., and Spudich, J.A. (1996) The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc. Natl. Acad. Sci. USA 93, 4459-4464
30. Dominguez, R., Freyzon, Y., Trybus, K.M., and Cohen, C. (1998) Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the pre-power stroke state. Cell 94, 559-571
31. Goldman, Y.E. (1998) Wag the tail: structural dynamics of actomyosin. Cell 93, 1-4
32. Molloy, J.E., Burns, J.E., Kendrick-Jones, J., Tregear, R.T., and White, D.C. (1995) Movement and force produced by a single myosin head. Nature 378, 209-212
33. Finer, J.T., Simmons, R.M., and Spudich, J.A. (1994) Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368, 113-119
34. Guilford, W.H., Dupuis, D.E., Kennedy, G., Wu, J., Patlak, J.B., and Warshaw, D.M. (1997) Smooth muscle and skeletal muscle myosins produce similar unitary forces and displacements in the laser trap. Biophys. J. 72, 1006-1021
35. Holmes, K.C. (1997) The swinging lever-arm hypothesis of muscle contraction. Curr. Biol. 7, R112-R118
36. Jontes, J.D., Wilson-Kubalek, E.M., and Milligan, R.A. (1995) A 32 degree tail swing in brush border myosin I on ADP release. Nature 378, 751-753
37. Kinose, F., Wang, S.X., Kidambi, U.S., Moncman, C.L., and Winkelmann D.A. (1996) Glycine 699 is pivotal for the motor activity of skeletal muscle myosin. J. Cell. Biol. 134, 895-909
38. Gollub, J., Cremo, C.R., and Cooke, R. (1996) ADP release produces a rotation of the neck region of smooth myosin but not skeletal myosin. Nat. Struct. Biol. 3, 796-802
39. Anson, M., Geeves, M.A., Kurzawa, S.E., and Manstein, D.J. (1996) Myosin motors with artificial lever arms. EMBO J. 15, 6069-6074
40. Waller, G.S., Ouyang, G., Swafford, J., Vibert, P., and Lowey, S. (1995) A minimal motor domain from chicken skeletal muscle myosin. J. Biol. Chem. 270, 15348-15352
41. Gollub, J., Cremo, C.R., and Cooke, R. (1999) Phosphorylation regulates the ADP-induced rotation of the light chain domain of smooth muscle myosin. Biochemistry 38, 10107-10118
42. Miller, L., Coppedge, J., and Reisler, E. (1982) The reactive SH1 and SH2 cysteines in myosin subfragment 1 are cross-linked at similar rates with reagents of different length. Biochem. Biophys. Res. Commun. 106, 117-122
43. Tao, T. and Lamkin, M. (1981) Excitation energy transfer studies on the proximity between SH1 and the adenosine triphosphatase site in myosin subfragment 1. Biochemistry 20, 5051-5055
44. Sutoh, K. (1981) Location of SH1 and SH2 along a heavy chain of myosin subfragment 1. Biochemistry 20, 3281-3285
45. Hiratsuka, T. (1988) Cross-linking of three heavy-chain domains of myosin adenosine triphosphatase with a trifunctional alkylating reagent. Biochemistry 27, 4110-4114
46. Ajtai, K. and Burghardt, T.P. (1989) Fluorescent modification and orientation of myosin sulfhydryl 2 in skeletal muscle fibers. Biochemistry 28, 2204-2210
47. Rajasekharan, K.N., Mayadevi, M., and Burke, M. (1989) Studies of ligand-induced conformational perturbations in myosin subfragment 1. An examination of the environment about the SH2 and SH1 thiols using a photoprobe. J Biol. Chem. 264, 10810-10819
48. Kasprzak, A.A., Chaussepied, P., and Morales, M.F. (1989) Location of a contact site between actin and myosin in the threedimensional structure of the acto-S1 complex. Biochemistry 28, 9230-9238
49. Hiratsuka, T. (1992) Movement of Cys-697 in myosin ATPase associated with ATP hydrolysis. J. Biol. Chem. 267, 14941-14948
50. Hiratsuka, T. (1993) Behavior of Cys-707 (SH1) in myosin associated with ATP hydrolysis revealed with a fluorescent probe linked directly to the sulfur atom. J. Biol. Chem. 268, 24742- 24750
51. Xing, J. and Cheung, H.C. (1995) Internal movement in myosin subfragment 1 detected by fluorescence resonance energy transfer. Biochemistry 34, 6475-6487
52. Phan, B.C., Peyser, Y.M., Reisler, E., and Muhlrad, A. (1997) Effect of complexes of ADP and phosphate analogs on the conformation of the Cys707-Cys697 region of myosin subfragment 1. Eur. J. Biochem. 243, 636-642
53. Patterson, B., Ruppel, K.M., Wu, Y., and Spudich, J.A. (1997) Cold-sensitive mutants G680V and G691C of Dictyostelium myosin II confer dramatically different biochemical defects. J. Biol. Chem. 272, 27612-27617
54. Lakowics, J.R. (1983) Principles of Fluorescence Spectroscopy, pp. 305-309, Plenum Press, New York
55. Miki, M., O'Donoghue, S.I., and DosRemedios, C.G. (1992) Structure of actin observed by fluorescence resonance energy transfer spectroscopy. J Muscle Res. Cell Motil. 13, 132-145
56. Perry, S.V. (1952) Myosin adenosine triphosphatase. Methods Enzymol. 2, 582-588
57. Weeds, A.G. and Taylor, R.S. (1975) Separation of subfragment-1 isoenzymes from rabbit skeletal muscle myosin. Nature 257, 54-56
58. Robson, R.M., Goll, D.E., and Temple, M.J. (1968) Determination of proteins in "Tris" buffer by the biuret reaction. Anal. Biochem. 24, 339-341
59. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
60. Maruta, S., Mizukura, Y., and Chaen, S. (2002) Interaction of a new fluorescent ATP analogue with skeletal muscle myosin subfragment-1. J. Biochem. 131, 905-911
61. Youngburg, G.E. and Youngburg, M.V. (1930) A system of blood phosphorus analysis. J. Lab. Clin. Med. 16, 158-166
62. Hiratsuka, T. (1999) ATP-induced opposite changes in the local environments around Cys697 (SH2) and Cys707 (SH1) of the myosin motor domain revealed by the prodan fluorescence. J. Biol. Chem. 274, 29156-29163
63. Prendergast, F.G., Meyer, M., Carlson, G.L., Iida, S., and Potter, J.D. (1983) Synthesis, spectral properties, and use of 6-Acryloyl-2-dimethylaminonaphthalene (Acrylodan). A thiol-selective, polarity-sensitive fluorescent probe. J. Biol. Chem. 258, 7541-7544
64. Chattopadhyay, A. (1990) Chemistry and biological of N-(7- nitrobenz-2-oxa-1,3-diazol-4-yl)-labeled lipids: fluorescent probes of biological and model membranes. Chem. Phya Lipids 53, 1-15
65. Burke, M., Reisler, E., Himmelfarb, S., and Harrington, W.F. (1974) Myosin adenosine triphosphatase. Convergence of activation by actin and by SH1 modification at physiological ionic strength. J. Biol. Chem. 249, 6361-6363
66. Burke, M. and Knight, P.J. (1980) Studies on the role of sulfhydryls in the myosin ATPase. Characterization of the site of modification by the bifunctional sulfhydryl reagent p-N,N′-phenylenedimaleimide. J. Biol. Chem. 255, 8385-8387
67. Miller, L., Coppedge, J., and Reisler, E. (1982) The reactive SH1 and SH2 cysteines in myosin subfragment 1 are cross-linked at similar rates with reagents of different length. Biochem. Biophys. Res. Commun. 106, 117-122
68. Perkins, W.J., Weiel, J., Grammer, J., and Yount, R.G. (1984) Introduction of a donor-acceptor pair by a single protein modification. Forster energy transfer distance measurements from trapped 1,N6-ethenoadenosine diphosphate to chromophoric cross-linking reagents on the critical thiols of myosin subfragment. J. Biol. Chem. 259, 8786-8793
69. Arata, T. (1986) Structure of the actin-myosin complex produced by crosslinking in the presence of ATP. J. Mol. Biol. 191, 107-116.
70. Houdusse, A., Kalabokis, V.N., Himmel, D., Szent-Gyorgyi, A.G., and Cohen, C. (1999) Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell 97, 459-470
71. Smyczynski, C. and Kasprzak, A.A. (1997) Effect of nucleotides and actin on the orientation of the light chain binding domain in myosin subfragment 1. Biochemistry 36, 13201-13207
72. Suzuki, Y., Yasunaga, T., Ohkura, R., Wakabayashi, T., and Sutoh, K. (1998) Swing of the lever arm of a myosin motor at the isomerization and phosphate-release steps. Nature 396, 380-383
73. Xiao, M., Li, H., Snyder, G.E., Cooke, R., Yount, R.G., and Selvin, P.R. (1998) Conformational changes between the active- site and regulatory light chain of myosin as determined by luminescence resonance energy transfer: the effect of nucleotides and actin. Proc. Natl. Acad. Sci. USA 95, 15309-15314
74. Highsmith, S. and Eden, D. (1990) Ligand-induced myosin subfragment 1 global conformational change. Biochemistry 29, 4087-4093
75. Sugimoto, Y., Tokunaga, M., Takezawa, Y., Ikebe, M., and Wakabayashi, K. (1995) Conformational changes of the myosin heads during hydrolysis of ATP as analyzed by x-ray solution scattering. Biophys. J. 68, 29S-34S
76. Howard, J. and Spudich, J.A. (1996) Is the lever arm of myosin a molecular elastic element? (Appendix to Ref 29). Proc. Natl. Acad. Sci. USA 93, 4462-4464
77. Warshaw, D.M., Guilford, W.H., Freyzon, Y., Krementsova, E., Palmiter, K.A., Tyska, M.J., Baker, J.E., and Trybus, K.M. (2000) The light chain binding domain of expressed smooth muscle heavy meromyosin acts as a mechanical lever. J. Biol. Chem. 275, 37167-37172
78. Yanagida, T. and Iwane, A.H. (2000) A large step for myosin. Proc. Natl. Acad. Sci. USA 97, 9357-9359
79. Tanaka, H., Homma, K., Iwane, A.H., Katayama, E., Ikebe, R., Saito, J., Yanagida, T., and Ikebe, M. (2002) The motor domain determines the large step of myosin-V Nature 415, 192-195